Title of Dissertation: the importance of female phenotype in determining reproductive potential and recruitment in atlantic coast striped bass




НазваниеTitle of Dissertation: the importance of female phenotype in determining reproductive potential and recruitment in atlantic coast striped bass
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Abstract


Title of Dissertation: THE IMPORTANCE OF FEMALE PHENOTYPE IN DETERMINING REPRODUCTIVE POTENTIAL AND RECRUITMENT IN ATLANTIC COAST STRIPED BASS (MORONE SAXATILIS)


Adam Christopher Peer, Doctor of Philosophy, 2012


Dissertation Directed by: Director and Professor Dr. Thomas J. Miller

University of Maryland Center for Environmental Science


The influence of female phenotype on the reproductive potential of Atlantic coast striped bass is addressed in three key areas of research. The importance of the environment in shaping maternal phenotype was evaluated using a spawning stock time-series to evaluate possible environmental drivers of female migration timing in the Chesapeake Bay. Results showed that local and recent water temperature was the primary factor influencing timing of movement onto spawning grounds, with higher temperatures resulting in early movements. Next, two approaches were used to evaluate the influence of female energetic condition on reproductive potential. First, a field approach was used to test the hypothesis that relative total female condition (hereafter condition) has a positive influence on pre-fertilized indicators of reproductive potential (i.e., probability of spawning, relative fecundity, and relative oocyte volume). Results indicated that condition had a positive influence on residual fecundity, residual oocyte volume and indirectly on the probability of spawning. In the second approach, a laboratory experiment was conducted to test the hypothesis that female condition has a positive effect on offspring size, growth and survival. The null hypothesis that the maternal influences on offspring phenotype did not differ in the Chesapeake Bay and Roanoke River populations also was tested. In contrast to the effects of female condition on pre-fertilized indicators of reproductive potential, condition had no influence on offspring phenotype in either population. Instead, post-spawn gutted weight alone had the greatest influence on offspring phenotype, although to a lesser and potentially insignificant degree in the Roanoke River.

Finally, a preliminary field evaluation was conducted in the Patuxent River, MD to determine whether maternal influences can lead to disproportionate numbers of mothers contributing to juvenile recruitment. Specifically, this study evaluated whether the variance in the distribution of half-sibling families was greater than expected by random reproductive success (i.e., Poisson process). If true, it was expected that the effective population size would be orders of magnitude smaller than the census size. Results provide preliminary evidence for higher than expected variance in reproductive success; however, methodological improvements will be necessary to confirm these results in the future.


THE IMPORTANCE OF FEMALE PHENOTYPE IN DETERMINING REPRODUCTIVE POTENTIAL AND RECRUITMENT IN ATLANTIC COAST STRIPED BASS (MORONE SAXATILIS)


by


Adam Christopher Peer


Thesis submitted to the Faculty of the Graduate School of the

University of Maryland, College Park in partial fulfillment

of the requirements for the degree of

Doctor of Philosophy

2012


Advisory Committee:


Professor Thomas J. Miller, Chair

Professor Edward D. Houde

Dr. Pierre Pepin

Professor Allen R. Place

Dr. Frank Siewerdt


©Copyright by

Adam Christopher Peer

2012

Foreward

According to the rules and regulations of the Graduate School of the University of Maryland, a graduate student may co-author work with faculty and colleagues that is included in a Dissertation. In such an event the University requires that a forward be included in the Dissertation, as approved by the Dissertation Committee, that clearly defines the substantial contributions the candidate made to the relevant aspects of the jointly authored work included in the Dissertation.

In accordance with the above, the Dissertation Committee approved the following statement of the candidate’s intellectual contribution to the dissertation. Chapters 1 and 6 are entirely the candidate’s own work. All of the remaining chapters are co-authored. Dr. Thomas Miller is co-author on all of these chapters. Dr. Miller offered constructive criticism on the design, analysis, interpretation and effective written communication of the research in addition to providing logistical support. The contributions of Dr. Miller to the Dissertation fall within the normal bounds of graduate supervision. Chapter 5 is co-authored with Dr. Miller and Dr. Allen R. Place, University of Maryland Center for Environmental Science. Dr. Place provided critical advice and direction in the development of the microsatellites used to evaluate sibling relationships. Further, many important editorial suggestions were provided by committee members Drs. Edward D. Houde, Pierre Pepin, Allen R. Place and Frank Siewerdt.

Dedication


This work is dedicated to several key individuals in my life. To Deborah for all of her love and support during this long and sometimes difficult road. To my mom and dad and brother and sister, for always believing in me and supporting all of my aspirations. To the memory of my faithful canine companion Sela, who kept me leveled headed throughout my graduate career. Finally, to the memories of my grandfathers Chester DiBari and Roy Peer, from whom I certainly inherited my curiosity for nature.

Acknowledgements


This work could not have been completed without guidance provided by Dr. T.J. Miller. I would like to thank Tom for allowing me to take some risks to further understand maternal influences in striped bass. Equally, Tom’s “pivot foot” analogy (passed down from Jim Rice) was invaluable in retaining a solid foundation for this dissertation. I would also like to thank my committee for their advice, constructive critiques and dedication to helping complete this project. Special thanks go to Dr. A. R. Place, as well as Ernest Williams for having the patience to train an ecologist the details of the molecular world. I would also like to thank Jason Edwards and David Loewensteiner for the their assistance and comaraderie in the field, expertise with a tire iron and sharing previously unknown humor of calling the Nottingham turkey. I would also like to thank Janet Nye for her scholarly advice and detailed reviews of several chapters. There were many people who helped in the lab and field and I would like to thank you all for your assistance, especially Casey Hodgkins for her mastery of the calorimeter and Mike Selckmann for his wizardry with fecundity and ovary color analysis. I would also like to thank all the people in the Miller lab group who helped edit my work.

Table of Contents

List of Tables vi

List of Figures ix

Chapter 1: Dissertation Introduction 1

Background 1

Environmental influences on female phenotype 6 The importance of energetic condition on striped bass reproductive potential 8

The importance of maternal influences in nature 11


Chapter 2: Local water temperature as a driver of changing migration phenology in Chesapeake Bay striped bass 24

Abstract 24

Introduction 25

Methods 30

Results 37

Temporal trends 37

Environmental and climatological correlations with d25, d50 and d75 and

IQRC 39

Environmental and climatological effects on d25, d50 and d75 41

Environmental influences on the proportion of egg-bearing females caught 43

Discussion 43


Chapter 3: The positive effects of relative energetic condition on female striped bass reproductive potential 82

Abstract 82

Introduction 83

Methods 88

Results 95

Relative total weight as an index of relative total energy 95

Size, age and relative condition demographics 96

Probability of spawning 97

Factors influencing residual fecundity 99

Factors influencing residual oocyte volume 100

Discussion 100


Chapter 4: Maternal size, but not energetic condition, influences progeny size, growth and survival in two populations of Atlantic coast striped bass (Morone saxatilis) 139

Abstract 139

Introduction 140

Methods 147

Results 160

Female, egg and 4-dph larval characteristics 160

Maternal influences on early-life characteristics 161

Egg influences on early-life characteristics 164

Population differences in maternal influences 167

Discussion 168

Chapter 5: Testing for evidence of maternal influences in a natural striped bass population: Lessons learned and challenges ahead. 205


Abstract 205

Introduction 206

Methods 212

Results 222

Discussion 226


Chapter 6: Summary and Conclusions 256


Appendix A 265


Appendix B 294


Appendix C 297


List of Tables


Table 2.1: Specific years of data that were included in the analysis for determining day of 25, 50, and 75% catch of female striped bass. The time-series available was from 1985-2010 69


Table 2.2: Pearson correlations of local environmental and large-scale climatic variables that showed significant relationships with day of 25, 50 and 75% catch for at least one striped bass female size class in the Upper Bay (a) and Potomac River (b). Significant (p < 0.05) relationships are shown in bold and nearly significant (0.08 > p > 0.05) relationships are italicized 70


Table 2.3: Standard deviations and factor loadings for the first 3 principal components of principal component analyses conducted on the local environmental and large-scale climatic variables shown to exhibit significant correlations (Table 2.2) with day of 25, 50 and 75% catch in the Upper Bay (a) and Potomac River (b) 71


Table 2.4: General linear model results showing the effects of individual local environmental variables from the Upper Bay region, large-scale climatic variables, and principal components on day of 25, 50 and 75% catch of female striped bass collected on the Upper Bay spawning grounds. Principal components (PC) were derived from the principal components analysis that included the individual variables shown below (see Table 2.3). Eta-squared coefficients (2) are shown for PCs or environmental variables that explained a significant proportion of the variance in respective components of the catch distribution 72


Table 2.5: General linear model results showing the effects of individual local environmental variables from the Potomac River region, large-scale climatic variables, and principal components on day of 25, 50 and 75% catch of female striped bass collected on the Potomac River spawning grounds. Principal components were derived from the principal components analysis that included the individual variables shown below (see Table 2.3). Eta-squared coefficients (2) are shown for PCs or environmental variables that explained a significant proportion of the variance in respective components of the catch distribution 73


Table 2.6: Tukey honestly significant difference test for multiple comparisons of mean differences in the day of 25, 50 and 75% catch among different female size classes of striped bass collected in the Upper Bay (a) and Potomac River (b). Comparisons are post-hoc results derived from the general linear models shown in Tables 2.3 and 2.4, which included PC2 and PC1 as covariates in the Upper Bay and Potomac River GLMs, respectively 74


Table 3.1:Female measures of energetic condition and their respective acronyms. All residuals come from the relationship between female total length and the respective weight or total tissue energy measured. 126


Table 3.2: General linear model results to evaluate if age (a), total length (b), gutted weight (c), residual total weight (d), residual gutted weight (e), residual ovary energy (f), residual liver energy (g), and residual visceral energy (h) vary by year, stage (i.e., reproductive stage) or calendar day of year (doy). Results for each model are shown in row format with p-value (italicized) shown below F-statistics. When interactions were significant in the analysis Type III SS were used and non-significant interactions were removed from the analysis (i.e., no results shown in table); otherwise, Type II SS were used and all interactions remained in the respective models. 127


Table 3.3:Generalized linear model (binomial error structure) results showing the influence of several condition indices, size and age on the probability of female striped bass spawning during 2009 and 2010 in the Chesapeake Bay. Likelihood ratio chi-square (LR 2) and degrees of freedom (df) are shown. 128


Table 3.4: General linear model results for evaluating whether residual fecundity varies between 2009 and 2010 (year), between reproductive stage 3 and 4 (stage) and by calendar day of year (doy). 129


Table 3.5:Linear model results for the effect of seven separate relative condition indices on striped bass residual fecundity. Each separate model is shown in row format, with the relative condition main effect designating the row for each separate model. Significant effects are shown in bold and all p-values are italicized. 130


Table 3.6: General linear model results for evaluating whether residual oocyte volume varies between 2009 and 2010 (year), between reproductive stage 3 and 4 (stage) and by calendar day of year (doy). 131


Table 3.7: Linear model results for the effect of seven separate relative condition indices on striped bass on residual oocyte volume. Each separate model is shown in row format, with the condition/feeding history main effect designating the row for each separate model. Significant effects are shown in bold and all p-values are italicized. 132


Table 4.1: Pearson correlations among female (all capital letters), egg and initial larval characteristics (all lower-case letters) from the Chesapeake Bay (white) and Roanoke River (gray) populations. Significant (p < 0.05) and nearly significant (0.05 ≥ p ≥ 0.07) correlations are indicated by enlarged and bold font and enlarged italicized font respectively. 195


Table 4.2: Repeated measures mixed model results for the Chesapeake Bay population, with larval characteristics as dependent variables and maternal characteristics as independent variables. Numerator and denominator (Kenward-Roger correction for repeated measures) degrees of freedom are shown as subcripts to t and F values. 196


Table 4.3: Repeated measures mixed model results for the Roanoke River population, with larval characteristics as dependent variables and maternal characteristics as independent variables. Numerator and denominator (Kenward-Roger correction for repeated measures) degrees of freedom are shown as subscripts to t and F values. 197


Table 4.4: Repeated measures mixed model results for the Chesapeake Bay population, with larval characteristics as dependent variables and egg characteristics as independent variables. Numerator and denominator (Kenward-Roger correcation for repeated measures) degrees of freedom are shown as subscripts to t and F values

198


Table 4.5: Repeated measures mixed model results for the Roanoke River population, with larval characteristics as dependent variables and egg characteristics as independent variables. Numerator and denominator (Kenward-Roger correction for repeated measures) degrees of freedom are shown as subscripts to t and F values. 199


Table 4.6: Repeated measures mixed model results with larval total length, weight, instantaneous growth in length and weight, and percent mortality as dependent variables and genetic population as the primary independent variable. Population and ration were binary variables with CB and high equal to 1, respectively. Numerator and denominator (Kenward-Roger correction for repeated measures) degrees of freedom are shown as subscripts to t and F values. 200


Table 5.1. Dates when striped bass eggs were collected by bongo net in the Patuxent River. 246


Table 5.2. Summary of microsatellite diversity and statistics for 5 loci evaluated in egg and juvenile striped bass collected in the Patuxent River. Shown are the number of alleles (n), rarefied estimates of allelic richness (AR), observed heterozygosity (Ho), expected heterozygosity (He), P-values for Hardy-Weinberg equilibrium (HWE) tests (Arlequin 3.1), heterozygote deficit and null allele frequencies (Genepop 4.0.10). Significant deviations from HWE and significant heterozygote deficit after sequential Bonferroni correction are indicated by an asterisk (*). 247


Table 5.3. P-values for genotypic disequilibrium between all pairs of loci for eggs and juveniles collected in 2007 and 2009. Significant genotypic disequilibrium after sequential Bonferroni correction for multiple tests is shown by an asterisk (*). 248


Table 5.4. Effective population size estimates when using 2 – 5 microsatellite loci. The asterisk indicates that uninformative (i.e., negative) values were produced. 249

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